Journal of Plant Protection Research ISSN 1427-4345

ORIGINAL ARTICLE

Developing an artificial diet for rearing Orius albidipennis Reuter (Het., )

Ali Rajabpour1*, Ali Asghar Seraj2, Amin Mehrnia3

1 Department of Plant Protection, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Khuzestan province, Iran 2 Department of Plant Protection, Shahid Chamran University of Ahvaz, Ahvaz, Khuzestan province, Iran 3 Department of Food Technology, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Ahvaz, Khuzestan province, Iran

Vol. 58, No. 3: 276–281, 2018 Abstract DOI: 10.24425/jppr.2018.124635 The use of suitable mass rearing methods is crucial to establish successful inundative or inoculative biological control programs. The development of an artificial diet consider- Received: May 17, 2018 ably reduces costs of mass rearing. In this study, the efficacy of a new meridic artificial Accepted: September 4, 2018 diet for rearing the predatory bug, Orius albidipennis (Het., Anthocoridae), was studied. The artificial diet was composed of some natural materials including lamb liver, hen yolk, *Corresponding addresses: [email protected]; whey protein, honey, royal jelly and some specific vitamins. To determine the artificial diet [email protected] efficacy life table parameters of the bugs, using the two-sex life table method, fed artificial and factitious diets, Ephestia kuehniella egg + date palm pollen, were compared. Results showed that O. albidipennis could complete its life stages and reproduce when reared on the recommended artificial diet. However, its fecundity and survival rate when fed the artificial diet was lower than the controls. Overall, due to lower production costs the artificial diet can be recommended for mass rearing of O. albidipennis despite the lower fecundity and survival rate. Keywords: anthocorid bugs, biological control, mass rearing, meridic diet, Orius albidipennis

Introduction

Minute pirate bugs (Het., Anthocoridae) are recog- eggs of pentatomids (Woodroffe 1973), eggs and larvae nized as potential biocontrol agents against many ar- of lepidopteran pests (Salehi et al. 2016) and thropod pests in different parts of the world (Omkar (Stansly 2010; Banihasemi et al. 2017). Orius albidipen- 2016). The bugs have economic importance due to their nis Reuter is a dominant species in many regions of high colonization rates, mobility, prey consumption Iran (Hassanzadeh et al. 2013). Some characteristics of efficacy and fecundity. Among various genera of the the species, including its ability to tolerate high tem- family Orius Wolff is the most important genus which peratures and lack of photoperiod induced diapauses, has worldwide distribution. These predatory bugs can make the predator an ideal candidate for mass rear- attack many soft body including thrips (Tom- ing and augmentative releases against many field and masini et al. 2004; Rajabpour et al. 2011), mites (Has- greenhouse pests in subtropical and tropical regions sanzadeh et al. 2015), (Akramovskaya 1978), (Sobhy et al. 2010). Ali Rajabpour et al.: Developing an artificial diet for rearing Orius albidipennis Reuter… 277

Usually, the success of inoculative or inundative Table 1. Composition of artificial diet for rearing Orius releases of natural enemies (NEs) depends on eco- albidipennis nomic and efficient mass-rearing programs (Bueno Ingredient Weight et al. 2006). Developing new methods for mass-rearing Distillated water 30 g a natural enemy reduces biological control costs (Bue- Lamb liver 50 g no et al. 2006; Safaei et al. 2015). Mass rearing methods for Orius continue to be improved by decreasing costs Fresh hen yolk 50 g and increasing efficiency of production as primary Whey protein (80%) 20 g goals (Shapiro and Ferkovich 2006). In the current Honey 25 g mass rearing methods for O. albidipennis and many Royal jelly 2 g other Orius bugs, lepidopteran eggs, especially Ephes- Ascorbic acid 1 g tia kuehniella Zeller (Lep., Pyralidae) eggs, and pollens Vitamin E 400 mg are used as a factitious diet (Bonte and De Clercq 2010; Safaei et al. 2015). The diet has many limitations since Vitamin A 300 µg it is relatively expensive and is available seasonally Thiamin (vitamin B1) 1 mg (Arijs and De Clercq 2004). Therefore, the availabil- Riboflavin (vitamin B2) 0.4 mg ity of a cheap and adequate artificial diet could lead to Niacin 8 mg a more economic large-scale rearing of the predators Vitamin B6 0.4 mg (Arijs and De Clercq 2004). Some artificial diets were Folic acid 55 µg previously reported for rearing some Orius preda- Vitamin B12 2 µg tory bugs including O. laevigatus Fieber (Arijs and De Clercq 2004; Bonte and De Clercq 2010), O. strigicollis Sesame oil 8 g Poppius (Lee and Lee 2004), O. sausteri Poppius (Tan Bean pod 20 g et al. 2013) and O. insidiosus Say (Ferkovich and Sha- Homogenized extract of Ephestia kuehniella egg 0.4 g piro 2004a, b). Date palm pollen 10 g However, there has been no effort to develop an ef- Gentamicin (as preservative) 3 mg fective artificial diet for mass rearing ofO. albidipennis. Therefore, the objective of this study was to develop an artificial diet and compare it with a factitious diet, which was obtained from the bodies of an were selected from various formulations. If fed including Ephestia eggs. other formulations the predatory bugs did not feed on them or they did not develop to the adult stage or reproduce. Materials and Methods Preparation and combination of the ingredients were done in the Food Science Laboratory of Ramin Agriculture and Natural Resources, University of collection Khuzestan. The ingredients were weighed with a pre- cise digital scale (AND model HR200). The ingredi- Orius albidipennis adults were collected from un- ents were mixed and homogenized with an electric sprayed sunflower fields in the Mollasani region, blender (Model track X, Black and Decker, USA) Khuzestan province, southwest Iran (31°36’01.5”N for 20 min (500 rounds per minute). Two millilit- 48°52’58.1”E). Female bugs were isolated in a plexiglas ers of the diet were taken in a microcentrifuge tube. cylinder (18 cm high, 7.5 cm diameter) covered with The tube opening was sealed with Parafilm® M. The a fine gauze lid on the top and margin for ventilation. The packed diet was stored in a freezer at –18°C when it bugs were reared on eggs of E. kuehniella + date palmat was not being used. 25°C (±1°C), 60% (±5%) RH (relative humidity), and 16 : 8 h (light : dark) in an incubator. Bean pod, Pha- seolus vulgaris L., was used as oviposition substrate. At Life table parameters least one male selected from the offspring was then One female and one male, 2 days old, were placed in identified by using keys of Woodroffe (1973). the plexiglas cylinder with a bean pod for 24 h, and then the bugs were removed. One egg was maintained Artificial diet on the pod and other eggs were removed by using a fine needle. The pod was placed in a rearing cylinder The compositions of the artificial diets for rearing with a tube of artificial diet at 25°C (±1°C), 60% (±5%) O. albidipennis are shown in Table 1. The compositions RH, and 16 : 8 h (light : dark) in an incubator. In the 278 Journal of Plant Protection Research 58 (3), 2018 control, 0.005 g of E. kuehniella egg + date palm pollen Table 2. Life history and life table parameters ± SE of Orius were used as a factitious diet. The insect was checked albidipennis reared on Ephestia kuehniella egg + date palm pollen and its life stages were recorded every day. After adult (control) and an artificial diet emergence, a fresh bean pod was placed in the cylinder Parameter [unit] Artificial diet Control every day. Each day, the number of eggs was recorded, Male longevity (day) 38.35 ± 0 .437 a 38.06 ± 0.799 a then the pod was transferred to a new container and Female longevity (day) 40.58 ± 0.641 a 39.95 ± 0.888 a replaced with another pod for oviposition. Observa- tions continued until bug death. Each treatment had APOP 2.642 ± 0.28 b 1.437 ± 0.155 a 40 replications. TPOP 24.357 ± 0.338 b 20.75 ± 0.429 a GRR 18.097 ± 3 b 30.792 ± 6.056 a Data analysis λ 1.093 ± 0.009 b 1.129 ± 0.0091 a r 0.089 ± 0.0082 b 0.121 ± 0.0081 a The life table and life history data of O. albidipennis m R 13.857 ± 3.162 b 26.558 ± 5.299 a fed an artificial diet and control bugs were analyzed 0 according to the theory of age-stage, two-sex life ta- T 29.488 ± 0.36 a 1.969 b ble (Chi and Liu 1985; Chi 1988). To facilitate data APOP – the period between the emergence of an adult female and her first analysis, life table analysis, and the bootstrap method, oviposition, TPOP – the time interval from birth to the beginning of ovi- position, GRR – the gross reproductive rate, λ – the finite rate of increase, a user-friendly computer program, TWOSEX-MS rm – intrisic growth rate, R0 – the net reproductive rate, T – the mean ge- Chart for the Windows operating system, was made neration time; the same letters in each row indicate non significant diffe- available at http://140.120.197.173/Ecology/prod02. rence (T-test) htm (Chi 2017). The age-stage specific survival rate

(sxj; where x – age and j – stage), the age-stage spe- cific fecundity (fxj), the age-specific survival rate (lx), control. However, GRR, λ, rm and R0 with artificial diet the age-specific fecundity (mx), and the population treatment were significantly lower than the control. l parameters [r – the intrinsic rate of increase; – the The values of GRR, λ, rm and R0 with control treat- r finite rate of increase (λ = e ); R0 – the net reproductive ment were 70.1, 3.29, 35.9 and 91.7% higher than ar- rate; T – the mean generation time] were calculated ac- tificial diet treatment. Also, the parameter T in artifi- cordingly. The bisection method can be found in most cial treatment was significantly (9.3%) more than the text books of numerical analysis (Burden and Faires control.

2005). The mean generation time is defined as the time Curves of age-specific survival rate (lx), age-specif- length that a population needs to increase to R0-fold ic fecundity of total population (mx), age-specific ma- of its size as the stable age-stage distribution and the ternity (lxmx), age-stage specific survival rate (sxj) and stable increase rate are reached. In other words, this age-stage life expectancy (exj) of O. elbidipennis reared rT T means e = R0 or λ = R0. The mean generation time on artificial diet and the control are presented in is calculated as T = (lnR0)/r. The gross reproductive Figures 1–3. rate (GRR) is calculated as GRR = Σmx. Also, the adult Curves of lx, mx and lxmx with artificial diet treat- pre-oviposition period (APOP – the period between ment are totally similar to the control. Moreover, the emergence of an adult female and her first oviposi- curve trends with artificial diet treatment and the tion), total pre-oviposition period (TPOP – the time control were similar. There was a difference between interval from birth to the beginning of oviposition) exj curves in artificial diet and the control. The age- were also calculated using the experimental data. Fi- stage life expectancy was extended to 46 days with nally, the standard errors and variances of the popula- artificial diet treatment in comparison with 52 day in tion parameters were estimated via the bootstrap tech- the control. nique (Efron and Tibshirani 1993), which is contained in the TWOSEX-MS Chart program. Sigma plot 12.5 was used to create graphs. Discussion

Results Our data indicated that O. albidipennis could complete its life stages and reproduce when reared on the rec- ommended artificial diet. However, its fecundity and Life table parameters of O. albidipennis reared on an survival rate when fed the artificial diet were lower artificial diet and controls are shown in Table 2. The than the control. results indicated that APOP and TPOP with artifi- The present results are in agreement with Arjis cial diet treatment were significantly more than the and De Clercq (2004) who showed that fecundity and Ali Rajabpour et al.: Developing an artificial diet for rearing Orius albidipennis Reuter… 279

Fig. 1. Curves of age-specific survival rate (lx), age-specific fecundity of total population (mx), age-specific maternity (lxmx) of Orius albidipennis reared on an artificial diet and the control

Fig. 2. Curves of age-stage specific survival rate (sxj) of Orius albidipennis reared on an artificial diet and the control

Fig. 3. Curves of age-stage life expectancy (exj) of Orius albidipennis reared on an artificial diet and the control

survival rate of O. laevigatus are reduced when fed maculiventris Say (Het., ) (Wittmeyer a liver based artificial diet in comparison with facti­ and Coudron 2001) fed an artificial diet. tious food, E. kuehniella egg. Similar results were ob- The lower fecundity of the predatory bug fed an ar- tained for O. strigicollis (Lee and Lee 2004) and Podisus tificial diet than the control may be due to the specific 280 Journal of Plant Protection Research 58 (3), 2018 lipid or protein content of E. keuhniella egg. Ferkovich tory bug, Orius laevigatus. Journal of Insect Science 10 (1): and Shaprio (2004b) showed that higher fecundity of 104. DOI: https://doi.org/10.1673/031.010.10401 Bueno V.H.P., Mendes S.M., Carvalho L.M. 2006. Evaluation O. insidiosus when fed Plodia interpunctata Hübner of a rearing-method for the predator Orius insidiosus. 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